10
RESEARCH ARTICLE Using landing statistics and fisherstraditional ecological knowledge to assess conservation threats to Pacific goliath grouper in Colombia Gustavo A. CastellanosGalindo 1,2 | Carolina ChongMontenegro 2 | Rodrigo A. Baos E 1 | Luis A. Zapata 1 | Paul Tompkins 2 | Rachel T. Graham 3 | Matthew Craig 4 1 World Wildlife Fund (WWF) Colombia, Programa Marino Costero, Cali, Colombia, South America 2 Leibniz Centre for Tropical Marine Research (ZMT), Bremen, Germany 3 MarAlliance, San Pedro, Belize 4 National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Southwest Fisheries Science Center, La Jolla, CA, USA Correspondence Gustavo A. CastellanosGalindo: World Wildlife Fund (WWF) Colombia, Programa Marino Costero, Carrera 35 No. 4 A 25, Cali, Colombia, South America. Email: [email protected] Funding information Conservation Leadership Programme (CLP); Rufford Foundation; WWF Colombia; Alexander von HumboldtStiftung Abstract 1. Groupers are vulnerable to fishing pressure largely because of their lifehistory traits. The Pacific goliath grouper (PGG; Epinephelus quinquefasciatus), the largest reef fish inhabiting the tropical Eastern Pacific region, is suspected to be subject to high levels of exploitation, but scarce information exists on their population status and the species remains classed as Data Deficient according to the International Union for Conservation of Nature (IUCN) Red List. 2. This study documents for the first time the threats to the PGG along the Colombian Pacific coast, where one of the few active fisheries for this species persists. Reconstructed landings of groupers and traditional ecological knowledge, gathered throughout several coastal villages, were used to obtain a historical and contemporary overview of the PGG status in Colombia. 3. Over the past 20 years grouper landings in the Colombian Pacific have been around 200 tons per year. Landings of PGG have averaged ~35 tons per year and are now close to matching those of the historically most landed grouper on this coast, the rooster hind (Hyporthodus acanthistius). The current smallscale fishery for PGG focuses on immature small individuals, with most taken from the extensive southern mangroves. Until recently fishers have captured PGG exclusively with handlines, but new fishing practices (spearfishing) and markets commanding higher prices for small individuals are increasing the extinction risk for the PGG. 4. The exploitation of PGG in the Colombian Pacific may not be as severe as in other countries where severe population declines are suspected (e.g. Mexico). Low coastal human population density and the presence of relatively intact mangroves, essential habitat for juvenile fishes, contribute to the persistence of PGG populations throughout the Colombian Pacific. 5. National and regional conservation and management measures should identify and protect mangrove nurseries and offshore spawning aggregation sites. Wellenforced protected nurseries and spawning aggregation sites will then protect juvenile and adult PGG, improving the sustainability of this fishery. KEYWORDS coastal, Colombia, conservation evaluation, Eastern Pacific, endangered species, fish, fishing, groupers, mangrove, red list, reef, urban development Received: 29 May 2017 Revised: 22 October 2017 Accepted: 5 December 2017 DOI: 10.1002/aqc.2871 Aquatic Conserv: Mar Freshw Ecosyst. 2018;110. Copyright © 2018 John Wiley & Sons, Ltd. wileyonlinelibrary.com/journal/aqc 1

Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

  • Upload
    others

  • View
    2

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

Received: 29 May 2017 Revised: 22 October 2017 Accepted: 5 December 2017

DOI: 10.1002/aqc.2871

R E S E A R CH AR T I C L E

Using landing statistics and fishers’ traditional ecologicalknowledge to assess conservation threats to Pacific goliathgrouper in Colombia

Gustavo A. Castellanos‐Galindo1,2 | Carolina Chong‐Montenegro2 | Rodrigo A. Baos E1 |

Luis A. Zapata1 | Paul Tompkins2 | Rachel T. Graham3 | Matthew Craig4

1World Wildlife Fund (WWF) Colombia,

Programa Marino Costero, Cali, Colombia,

South America

2Leibniz Centre for Tropical Marine Research

(ZMT), Bremen, Germany

3MarAlliance, San Pedro, Belize

4National Oceanic and Atmospheric

Administration, National Marine Fisheries

Service, Southwest Fisheries Science Center,

La Jolla, CA, USA

Correspondence

Gustavo A. Castellanos‐Galindo: World

Wildlife Fund (WWF) Colombia, Programa

Marino Costero, Carrera 35 No. 4 A 25, Cali,

Colombia, South America.

Email: [email protected]

Funding information

Conservation Leadership Programme (CLP);

Rufford Foundation; WWF Colombia;

Alexander von Humboldt‐Stiftung

Aquatic Conserv: Mar Freshw Ecosyst. 2018;1–10.

Abstract1. Groupers are vulnerable to fishing pressure largely because of their life‐history traits. The

Pacific goliath grouper (PGG; Epinephelus quinquefasciatus), the largest reef fish inhabiting the

tropical Eastern Pacific region, is suspected to be subject to high levels of exploitation, but

scarce information exists on their population status and the species remains classed as Data

Deficient according to the International Union for Conservation of Nature (IUCN) Red List.

2. This study documents for the first time the threats to the PGG along the Colombian Pacific

coast, where one of the few active fisheries for this species persists. Reconstructed landings

of groupers and traditional ecological knowledge, gathered throughout several coastal

villages, were used to obtain a historical and contemporary overview of the PGG status in

Colombia.

3. Over the past 20 years grouper landings in the Colombian Pacific have been around 200

tons per year. Landings of PGG have averaged ~35 tons per year and are now close to

matching those of the historically most landed grouper on this coast, the rooster hind

(Hyporthodus acanthistius). The current small‐scale fishery for PGG focuses on immature

small individuals, with most taken from the extensive southern mangroves. Until recently

fishers have captured PGG exclusively with handlines, but new fishing practices

(spearfishing) and markets commanding higher prices for small individuals are increasing

the extinction risk for the PGG.

4. The exploitation of PGG in the Colombian Pacific may not be as severe as in other countries

where severe population declines are suspected (e.g. Mexico). Low coastal human population

density and the presence of relatively intact mangroves, essential habitat for juvenile fishes,

contribute to the persistence of PGG populations throughout the Colombian Pacific.

5. National and regional conservation and management measures should identify and protect

mangrove nurseries and offshore spawning aggregation sites. Well‐enforced protected

nurseries and spawning aggregation sites will then protect juvenile and adult PGG, improving

the sustainability of this fishery.

KEYWORDS

coastal, Colombia, conservation evaluation, Eastern Pacific, endangered species, fish, fishing,

groupers, mangrove, red list, reef, urban development

Copyright © 2018 John Wiley & Sons, Ltd.wileyonlinelibrary.com/journal/aqc 1

Page 2: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

2 CASTELLANOS‐GALINDO ET AL.

1 | INTRODUCTION

Groupers (Epinephelidae) are a group of 168 species of small‐ to large‐

bodied teleost fishes that inhabit coastal habitats, where they play

important roles in coastal ecosystems as top predators (Craig, Sadovy

de Mitcheson, & Heemstra, 2011; Hixon & Carr, 1997; Stewart &

Jones, 2001). Under increasing pressure from coastal fisheries, grou-

pers are in demand because of their high value in local and interna-

tional markets (Craig et al., 2011; Heemstra & Randall, 1993).

Currently, 12% of groupers worldwide are considered under threat of

extinction (i.e. Critically Endangered, Endangered, or Vulnerable), with

another 13% considered as Near Threatened. Using the International

Union for Conservation of Nature (IUCN) Red List criteria, insufficient

data exist to complete any assessments for 30% of the species, and

these are listed as Data Deficient (Sadovy de Mitcheson et al., 2013).

Only four grouper species exceed 2 m in total length, including the

giant grouper (Epinephelus lanceolatus), Atlantic and Pacific goliath

groupers (Epinephelus itajara and Epinephelus quinquefasciatus, respec-

tively), and the Warsaw grouper (Hyporthodus nigritus) (Craig et al.,

2011). The Atlantic goliath grouper (E. itajara) is the largest reef fish

in the Western Hemisphere, and was long considered a single species

with a distribution on both tropical coasts of the Americas (Eastern

Pacific and Western Atlantic, including the Caribbean). Atlantic and

Pacific goliath groupers are now considered two genetically distinct

yet morphologically similar species, divided by the Isthmus of Panama

(Craig et al., 2009).

The Atlantic goliath grouper is assessed as Critically Endangered

based on its vulnerable life‐history characteristics and the observed

population declines in its distribution range over the past three gener-

ations (Craig et al., 2011; Graham, Rhodes, & Castellanos, 2009;

Sadovy & Eklund, 1999). The species is currently protected and har-

vesting is prohibited in the USA and Brazil; however, they are not

protected in many of the other countries in which they occur. Goliath

groupers in Colombia (Caribbean and Pacific coasts) were once

assessed as Critically Endangered based solely on anecdotal informa-

tion from the Colombian Caribbean coast (Mejía & Acero, 2002). After

the recognition of Atlantic and Pacific populations of goliath groupers

as distinct species (Craig et al., 2009), a regional assessment of the

Pacific species was completed in 2011 (Erisman, 2011), and this

suggested that the Pacific goliath grouper (hereafter PGG) had also

suffered severe declines over the past three decades throughout its

geographical range (from Mexico to Peru). The assessment acknowl-

edged the scarcity of fisheries‐independent data to determine the

species abundance, and relied on data for species population size and

current threats from the Gulf of California in Mexico and Panama.

Information from other countries was absent (Erisman, 2011; Polidoro

et al., 2012). For this reason, the PGG is now among the 50 species of

groupers for which a lack of sufficient information prevents an

adequate evaluation of populations (i.e. species listed as Data

Deficient; Sadovy de Mitcheson et al., 2013). Despite documenting

an active fishery for this species in Colombia (Baos, Castellanos‐

Galindo, Chong‐Montenegro, Tompkins, & Zapata, 2016), a recent

national assessment concluded that there is still insufficient informa-

tion to list E. quinquefasciatus under any other Red List category than

Data Deficient (Castellanos‐Galindo, Baos, & Zapata, 2017).

Assuming that Atlantic and Pacific goliath groupers have similar

life‐history characteristics, it can be expected that the extensive man-

grove areas in the Eastern Pacific, especially those in the Colombian

and Panamanian Pacific rainy coasts, may be a preferred habitat for

juveniles (of <110 cm total length, TL; Frias‐Torres, 2006; Koenig,

Coleman, Eklund, Schull, & Ueland, 2007; Sadovy & Eklund, 1999),

which will later migrate to deeper areas in adjacent reefs. The man-

grove areas in this region sustain important small‐scale fisheries

targeting largely shallow‐water estuarine fish species, potentially

including small‐sized PGGs. The degree of pressure placed on this spe-

cies by these small‐scale fishery fleets, however, is not yet known.

Investigating the dynamics of these fisheries is therefore likely to bring

insights into the fishery and biology of PGG in the Eastern Pacific.

In light of significant data gaps on fish and fisheries, traditional

ecological knowledge (TEK) or information gathered from fishers about

the local marine environment (Johannes, 1998) has the potential to

inform fisheries science (Hind, 2015). Johannes (1998) and Heyman

and Graham (2000a, 2000b, 2000c) encouraged decision makers and

scientists to validate and value TEK for marine species and fisheries

management and conservation. Beaudreau and Levin (2014) compared

TEK about fish abundance trends in Puget Sound, USA, from different

resource users in an attempt to synthesize qualitative and quantitative

knowledge about data‐poor species. Combining such valuable informa-

tion from resource users with standard quantitative fisheries data

could be a better way to correctly reconstruct marine species’ history

of exploitation, without the risk of falling into ‘shifting baseline

syndrome’ (Gaspari, Bryceson, & Kulindwa, 2015; Sáenz‐Arroyo,

Roberts, Torre, Cariño‐Olvera, & Enriquez‐Andrade, 2005).

This study attempts to provide a retrospective and up‐to‐date

account of Colombia's PGG fishery, probably one of the last areas in

the Eastern Pacific where an active fishery for this species exists

(Figure 1). The study involves: (i) a reconstruction of the official landing

statistics for groupers; (ii) monitoring of landings at the main small‐

scale fishery port between 2012 and 2015; and (iii) TEK gained from

fishers along coastal areas with different levels of anthropogenic

influence. The combination of these three sources of information pro-

vides the first account of the threats that this species faces in the

Colombian Pacific, and provides much needed fisheries and biological

information to determine the national and regional extinction risk for

this species (i.e. IUCN red listing in the tropical Eastern Pacific region).

2 | METHODS

2.1 | Study area

Colombia is located in north‐western South America, and is bordered

by the Pacific Ocean and the Caribbean Sea (1400 and 1600 km,

respectively; Correa & Morton, 2010). The Colombian Pacific coast

has a narrow continental shelf and is dominated by extensive man-

grove forests (predominantly Rhizophora spp. trees) in the south

(Castellanos‐Galindo, Cantera, Saint‐Paul, & Ferrol‐Schulte, 2015) and

rocky shores in the north, with very few coral reefs (Glynn & Ault,

2000). Annual rainfall fluctuates between 3000 and 10 000 mm along

the coast (Correa & Morton, 2010; Poveda & Mesa, 2000). Human

Page 3: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

FIGURE 1 Goliath groupers captured by speargun fishers between 1990 and 2015 at different localities of the Colombian Pacific coast: (a, b)individuals captured on the northern coast (Nuquí and Bahía Solano); (c, d) individuals captured on the central coast (near Juanchaco)

CASTELLANOS‐GALINDO ET AL. 3

development on the Colombian Pacific coast is extremely low

compared with the Caribbean (Ramírez & de Aguas, 2015), with only

two access roads connecting inland cities to the coast (Buenaventura

and Tumaco), and with all other areas accessible only by boat or small

airplanes (Figure 2).

2.2 | Marine fisheries in Colombia

Despite reports, the actual overall fishery catches in Colombia

(Caribbean and Pacific) may be twice the numbers reported by the

country to the Food and Agriculture Organization of the United

Nations (FAO), although they are relatively small in a global context

and contribute relatively little to the GDP of the country (less than

US $230 million per year in gross revenues; Wielgus, Zeller,

Caicedo‐Herrera, & Sumaila, 2010). Small‐scale fisheries are currently

responsible for the majority of the seafood that is consumed in the

country, with gross revenues for this sector of the Colombian Pacific

generally in the range of US $10–20 million per year. A major prob-

lem for fisheries management in Colombia is that official landing sta-

tistics combine multiple species into single categories (e.g. ‘groupers’),

thereby complicating or rendering impossible species‐level assess-

ments (Wielgus et al., 2010). This problem holds true for Pacific

Colombian groupers that are frequently lumped into the category

‘meros, chernas, and cabrillas’, despite comprising a group of

between eight and 10 species.

2.3 | Reconstruction of historical landings and recentmonitoring

As an initial step, ‘grouper’ (i.e. the ‘meros, chernas, and cabrillas’

category) and PGG landings from the Pacific coast were reconstructed

from data collected by the Colombian Fisheries Authority [Ministry

of Agriculture and Rural Development, Instituto Nacional de

Pesca y Acuicultura (INPA), Instituto Colombiano de Desarrollo Rural

(INCODER), Instituto Colombiano Agropecuario (ICA), and Autoridad

Nacional De AcuiculturaY Pesca (AUNAP)] from 1981 to 2015 (MADR

& CCI, 2011; Pereira‐Velásquez, 1993). These data correspond mainly

to the three main fish landing ports on the Colombian Pacific coast

where the Fisheries Authority undertakes monitoring, i.e. Tumaco,

Buenaventura, and Bahía Solano (Figure 2). This information was

complemented with detailed monitoring of PGG landings at the main

landing sites in Buenaventura from 2012 to 2015. During this period,

PGG landed at Pueblo Nuevo – the main landing site for small‐scale

fisheries in the Colombian Pacific – were measured (TL, to the nearest

Page 4: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

FIGURE 2 Map of the Colombian Pacific coast. Mangrove areas along the coast are indicated in green. National Parks (PNNs) are the areas in red.Shadowed areas correspond to Pizarro (red), San Juan (yellow), Juanchanco (dark blue), Naya (light green), and Sanquianga (light blue)

4 CASTELLANOS‐GALINDO ET AL.

0.1 cm) and weighed (to the nearest 0.1 kg). The reconstructed histor-

ical landings allowed an evaluation of the magnitude of grouper

catches in the Colombian Pacific over time, whereas detailed monitor-

ing between 2012 and 2015 provided insights into the size structure of

PGG landings and the predominant fishing grounds along the

Colombian Pacific coast. Based on these data, five broad areas along

the Colombian Pacific coast were defined (Juanchaco, Naya, Pizarro,

San Juan, and Sanquianga; Figure 2).

Page 5: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

CASTELLANOS‐GALINDO ET AL. 5

2.4 | Traditional ecological knowledge

Information from fishers capturing PGG was gathered at eight coastal

villages (northern region: Bahía Solano, Tribugá, Nuquí, Jurubirá, El

Valle, and Arusí; southern region: Bahía Málaga and Bazán) along the

Colombian Pacific coast. Semi‐structured interviews were used follow-

ing an adaptation of the survey methods used by Gerhardinger,

Marenzi, Bertoncini, Medeiros, and Hostim‐Silva (2006) in Brazil to

obtainTEK for the Atlantic goliath grouper. This ensured the compara-

bility of fishers’ attitudes between Brazil and Colombia. After visiting

each village and talking to recognized local leaders, fishers with

experience in fishing PGG were approached and interviewed. Topics

covered during interviews focused on: (i) the fisher's general informa-

tion and habits; (ii) knowledge of the biology and ecology of PGG; (iii)

perceptions of PGG conservation; and (iv) the socio‐economics of

PGG fisheries (Table 1).

3 | RESULTS

3.1 | Reconstruction of historical landings

Groupers in the Colombian Pacific are currently almost exclusively

targeted by small‐scale fishers. Total grouper landings (category ‘meros,

chernas, and cabrillas’) over the reconstructed period were extremely

variable, probably reflecting a lack of monitoring by fisheries authorities

in some years. For example, low landing values in 2002 and 2012 were

most likely the result of very limited monitoring during transitions in

management responsibilities between different government agencies.

Nevertheless, landings for this group for most years during 1981–2015

TABLE 1 Semi‐structured interviews designed to gather traditional ecologJurubirá, Arusí, Bahía Solano, and Bazán)

General topics Specific questions

General information Name, ageHow many years of fishing experience do you have?How did you start fishing? Who taught you?What kind of fishing do you normally practice? Whic

Goliath grouper fishing What kind of fishing technique do you know is approuse? What other techniques have you observed fr

What season or specific conditions are good to fish gWhat has been the largest goliath grouper that you hIs it possible to capture goliath groupers throughoutWhat is the cost of a goliath grouper fishing trip?It is profitable to fish goliath groupers?How many kinds of goliath groupers do you know?

Goliath grouper'sbiology

Have you observed or captured goliath groupers witIs it possible to differentiate between a male and a fDo you know what an adult goliath grouper eats? ADo you know if goliath groupers produce any kind oDo you know where juvenile and adult goliath groupAre goliath groupers aggressive? Are they aggressiveHave you captured or seen several goliath groupers

Goliath grouperperceptions

Do you perceive that there were more goliath groupcurrent abundance with that of some years ago?)

Do you think that goliath groupers face any threat?What do you think negatively affects or will affect thDo you think goliath groupers are important in the e

Socio‐economicaspects

What is the price of goliath grouper meat? To whomWhat other parts of the goliath grouper do you eat oAre there any beliefs or myths around the goliath groIs there any other name given to the goliath grouper

were below 250 t (mean = 213.6 t, standard error = 34.9 t; Figure 3).

Hyporthodus acanthistius, the rooster hind (cherna roja in Spanish),

together with the PGG E. quinquefasciatus (‘mero’) have been the two

most important groupers landed in the Colombian Pacific since at least

the year 2000. According to the national fishing statistics, between

2012 and 2015 these two species accounted for 64–93% of all grouper

landings. The average annual landings of rooster hind and PGG in 1995–

2015were 68.8 ± 4.6 t (±SE) and 34.5 ± 6.0 t, respectively (Figure 4). The

importance of both rooster hind and PGG in the overall landings of

grouper, however, has changed in recent years (since 2009). Whereas

rooster hind landings between 1995 and 2000 were between two‐ and

ten‐fold higher than those of PGG, in the last 8 years landings of both

species have been very similar, sometimes being even higher for PGG

(e.g. 2009 and 2010; Figure 4).

3.2 | Monitoring of fish market landings inBuenaventura

From July 2012 to December 2015, a total of 1981 PGG landed in the

fish market of Pueblo Nuevo were measured and weighed. The total

weight of grouper landings was 14 867.6 kg. Sizes ranged from 11.3

to 190.5 cm TL and from 0.3 to 110.0 kg in gutted weight. Mean TL

and weight (±SE) were 72.2 cm (±0.5 cm) and 7.6 kg (±0.2 cm), respec-

tively. PGG are landed and gutted in Pueblo Nuevo, and therefore no

information on food habits or reproduction could be gathered at this

landing site. Only 6% of the landed PGG were >110 cm TL, the size

at sexual maturity reported for E. itajara by Bullock, Murphy,

Godcharles, and Mitchell (1992). These patterns were consistent

throughout the years of monitoring (Figure 5). For 1428 of the landed

ical knowledge (TEK) from fishers at the five study sites (Bahía Malaga,

h are your most common target species?

priate/effective to fish goliath groupers? What fishing technique do youom other fishers?oliath groupers?ave fished or seen?the year? In which areas? Are these areas always the same?

h eggs? In what season? What size were these goliath groupers?emale in goliath groupers? In which manner?juvenile?f sound? Have you heard this?ers occur?in a specific season?at the same place and the same time? When? Where? What size?

ers in the past when you started fishing? How would you compare their

e survival of goliath groupers?cosystem? Do you know what role they play where they live?

do you sell it? Do you eat it?r use?uper?within your locality?

Page 6: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

FIGURE 3 Fish landings of groupers (Epinephelidae) in the Colombian Pacific, as reported by fisheries authorities from 1981 to 2015. Data from1981–1986 are taken from Pereira‐Velásquez (1993). Data from 1995–2010 are taken from Instituto Nacional de Pesca y Acuicultura (INPA),Instituto Colombiano de Desarrollo Rural (INCODER) and Corporación Colombia Internacional (CCI) official statistics. Data from 2012–2015 arefrom Servicio Estadístico Pesquero Colombiano (SEPEC; http://sepec.aunap.gov.co)

FIGURE 4 Reconstruction of landings of the two most important grouper species in the Colombian Pacific coast from 1995 to 2015 (Hyporthodusacanthistius and Epinephelus quinquefasciatus), as reported by the official statistics. Missing data from 2007–2009 indicate that statistics were notdifferentiated by species, whereas no official statistics are available for the 2011–2012 period

6 CASTELLANOS‐GALINDO ET AL.

specimens it was possible to identify the fishing ground: 60% came

from the southern area of Sanquianga, whereas 25% came from

Juanchaco on the central Colombian Pacific coast. The remaining three

fishing grounds contributed less than 10% of the total landed PGG

(Figure 6). The distribution of size classes for most fishing grounds

was largely represented by individuals of 50–100 cmTL. The exception

to this pattern was in Juanchaco, where specimens larger than 100 cm

TL were more common.

3.3 | Fishers’ traditional ecological knowledge

Forty‐six interviews (83% handline fishers, n = 38; 17% spear fishers, n

= 8) were conducted at different small villages on the Colombian

Pacific coast between 2010 and 2015. The fishing experience of the

interviewees varied: 20–30 years (9%), 31–40 years (22%),

41–50 years (28%), and >50 years (41%). PGG are captured all year

round; however, the interviewees identified two distinct times of the

year when landings were higher – August and May. Fishers generally

agreed that the better fishing in May was associated with the migra-

tion of the Pacific anchoveta (Cetengraulis mysticetus), which appar-

ently causes its predator, the PGG, to be more readily caught.

Irrespective of the season, 63% of fishers agreed that the best time

to catch PGG is during the 3 days around the peak of spring tides

(locally referred to as ‘puja’). Fishers argued that the PGG only feeds

during this portion of the tidal/lunar cycle.

3.3.1 | Knowledge of the biology and ecology of PGG

Seventy‐two percent of those interviewed could not identify any sexual

dimorphism in PGG, although 26% described females as shorter and

Page 7: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

FIGURE 5 Size structure of goliath groupers landed (n = 1981) from 2012 to 2015 at the principal landing sites in Buenaventura, on the ColombianPacific coast, tropical Eastern Pacific. Dashed lines indicate the approximate size at which ontogenetic shifts occur in goliath groupers in theAtlantic Ocean (juveniles to adults; ~100 cm TL) according to Frias‐Torres (2006) and Koenig et al. (2007)

FIGURE 6 Violin plot indicating the median sizes of goliath groupers caught in different regions along the Colombian Pacific coast (see Figure 2).The plot also shows the size distribution of individuals between fishing grounds. The dashed lines indicates the approximate size at which

ontogenetic shifts occur in goliath groupers in the Atlantic Ocean (juveniles to adults; ~100 cmTL) according to Frias‐Torres (2006) and Koeniget al. (2007)

CASTELLANOS‐GALINDO ET AL. 7

‘fatter’ and males as more elongated. Forty‐six percent of the inter-

viewees had never seenmature females of PGG, whereas 43% had only

observed eggs once or rarely. The reproductive season and length at

maturity is therefore unclear. Handline fishers identified black skipjack

(patiseca, Euthynnus lineatus) as the preferred food of the PGG, and this

was the fish species most commonly used as bait (52%).

The emission of loud, abrupt, and low‐frequency sounds by PGG

was acknowledged by 76% of the informants. The most experienced

fishers could use the unique sound made by the PGG to determine

the approximate location of the fish.

Most fishers agreed that ‘juvenile’ PGG prefer to live in shallow

estuarine habitats with high structural complexity (e.g. mangrove roots,

Page 8: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

8 CASTELLANOS‐GALINDO ET AL.

logfalls), whereas ‘adults’ prefer to live in or near shallow (<30 m)

offshore rocky reefs of high complexity (caves, rocky reefs, wrecks,

etc.). Eighty‐five percent of those interviewed agreed that PGG expe-

rience an ontogenetic habitat shift from estuarine to offshore habitats,

which is consistent with that of the Atlantic goliath grouper. PGG

behaviour in general was described as passive (61%), although

spearfishers described aggressive behaviour after a failed shot, with

the fish swimming towards them in self‐defence or to attack. During

one such incident, one spearfisher interviewed reported being half‐

swallowed headfirst and released, an account corroborated by several

other local fishers.

3.3.2 | Perceptions on PGG conservation

Most fishers (89%) agreed that there has been a decline in the local

PGG population over time. This decline is mainly attributed to

increased fishing effort (with an increasing number of fishers in the

area) and newly introduced spearfishing methods; however, 9% of

the interviewees (all of them spearfishers) agreed that there have not

been any changes in the population size, and that they have witnessed

recent large aggregations (>20 individuals) of adult PGG near Cabo

Corrientes and Cabo Marzo on the northern rocky coast of the

Colombian Pacific (Figure 1). Despite the perception of declines in

the PGG population, the overall fisher responses showed no clear

indications of declines in the size at catch or in the number of fish

caught to suggest a shifting baseline syndrome situation.

3.3.3 | Socio‐economics of PGG fisheries

In the northern area of Cabo Corrientes PGG is sold on average for US

$2 per kilo (gutted fish), no matter the size of the fish. In the southern

part (Bahía Málaga and Guapi) of the study area, which is closest to the

main market (Buenaventura), PGG weighing between 2.5 and 25.0 kg

(i.e. smaller immature individuals) fetch a better market price (US $3.7

per kilo) than individuals that weigh >25 kg (US $1.8 per kilo). Fishers

normally associate larger PGG individuals with tougher flesh. For most

fishers, PGG are not a targeted resource, but are rather occasionally

and opportunistically caught, which is reflected in the low market

prices compared with other more valuable species (e.g. snappers).

4 | DISCUSSION

An active Pacific goliath grouper fishery in the tropical Eastern Pacific

has not previously been reported upon. Findings indicate that the PGG

has increased its representation in overall grouper landings on the

Colombian Pacific coast over the last 15 years. The fishery for PGG

is currently as important in catches as that for the rooster hind, which

has been historically the most important targeted grouper species in

the region. Although the TEK from fishers does not indicate serious

declines in PGG populations, an increasing fishing effort on immature

fish could eventually lead to growth overfishing, and represents a

warning signal to regulate fisheries for this species. Equally worrying

is the apparent increase in spearfishing in some regions of the

Colombian Pacific (e.g. northern and central coasts). Spearfishers

normally target large and old PGG (Figure 1). Targeting this part of

the stock is increasingly recognized for generating size and age

truncation (Hixon, Johnson, & Sogard, 2014), which in turn reduces

the productivity and stability of marine communities (Barnett, Branch,

Ranasinghe, & Essington, 2017).

Grouper fisheries in the Colombian Pacific coast have been

formally documented since the 1980s by fishing authorities, although

several species of this group have been traditionally harvested by

small‐scale fishers prior to 1980. Landing values of ~400 tons per year

at the beginning of that decade contrast with the current landing

values of below 200 tons per year. This apparent decline should be

interpreted with caution as official landing statistics have been irregu-

larly collected throughout the years; however, if it is assumed that the

accessibility to landing sites and data gathering has increased over the

years, the decline in landings suggests a declining PGG fishery.

In the 1990s, a semi‐industrial fleet targeting four different grouper

species in the Colombian Pacific was active (Gómez & Zapata, 1999).

Olive grouper (Epinephelus cifuentesi) and rooster hind were the target

species of this fleet, whereas PGG were poorly represented in catches.

Since 2000, after an apparent collapse of this semi‐industrial fishery,

most grouper landings in the Colombian Pacific comprise rooster hind

and PGG (Figure 4). PGG landings in the Colombian Pacific remained

relatively constant between 1995 and 2006, with landings usually not

exceeding 50 tons per year (except for the years 2000 and 2001). These

catch values are around 10 times lower than those reported for the

Atlantic goliath grouper on the entire Brazilian coast (393 ton per year;

Giglio, Bertoncini, Ferreira, Hostim‐Silva, & Freitas, 2014), where this

species is protected from fishing by law but the enforcement seems to

be weak (Giglio et al., 2014). It is likely, however, that the PGG landing

values for the Pacific Colombian coasts are the highest of all countries

in the Eastern Pacific where PGG is distributed.

The increase in PGG landings (up to 80 tons per year) in 2009 and

2010 may be indicative of a greater fishing effort on this species. This

increase is potentially driven by the demand of the national market,

especially in the largest cities of the country (Cali, Bogotá, and

Medellín), and even on the Caribbean coast of Colombia where there

is a demand for grouper fillet from the tourism sector. Of special

concern is the fact that fish retailers prefer small, immature PGG,

which fetch considerably higher prices in the market. This is in contrast

to what was found in Belize by Graham et al. (2009), where larger

groupers provide greater income to fishers.

Information provided by the TEK of fishers helps to fill in some

knowledge gaps about basic PGG biological aspects, and provides

insights into the perceived long‐term trends in catches and abundances

of the PGG, especially in the northern area of the Colombian Pacific

coast. Similarities in the biological characteristics of the PGG and the

Atlantic goliath grouper (Aguilar‐Perera, González‐Salas, Tuz‐Sulub, &

Villegas‐Hernández, 2009; Frias‐Torres, 2006), such as ontogenic

habitat shifts and sound production, were observed. Interestingly, most

fishers were not aware of the reproductive cycle of PGG.

On the northern Colombian Pacific coast, the PGG fishery has been

discouraged by non‐governmental organizations (NGOs) claiming that

the PGG is currently at risk of extinction, although apparently this is

caused by confusion with the conservation status of the Atlantic goliath

grouper (Epinephelus itajara). This has decreased the overall fishing

pressure on this resource in this region; however, at the southern

coast's main landing port of Buenaventura, the PGG is currently actively

Page 9: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

CASTELLANOS‐GALINDO ET AL. 9

landed, although not targeted, as fishers tended to pursue other species

that are more readily caught and command better prices.

The prevailing environmental and socio‐economic conditions in

the Colombian Pacific region (e.g. highest rainfall in the Americas), high

mangrove densities, and low human population densities, may have all

combined to mitigate against severe population declines in PGG in

Colombia. The Colombian Pacific is sparsely populated (with five

inhabitants per km2; Meisel Roca & Pérez V, 2006), and therefore

fishing pressure is thought to be low compared with other coastal

regions in the tropical Eastern Pacific.

Although PGG exploitation along the Pacific coast of Colombia

and its effects on the populations appear to be not as severe as those

observed in other areas of the region (i.e. the Gulf of California;

Aburto‐Oropeza, Erisman, Valdez‐Ornelas, & Danemann, 2008), the

current signs of increased exploitation, higher demand from the local

market (especially of juvenile individuals), and introduction of fishing

gear that target large individuals (i.e. spearfishing), are warning signals

for the future of this species in Colombia, and indicate that conserva-

tion action is a priority. The Colombian Government's planned devel-

opments along the Pacific coast (e.g. new harbours and roads that

lead to human population increase and loss of critical habitat) in the

near future are likely to increase the pressure on fishery resources

and vulnerable species such as the PGG.

Implementing realistic conservation and management measures is

not an easy task in countries like Colombia, where fisheries are not

priorities for central governments. Nevertheless, measures that protect

or limit the catch of juvenile and very old fish could greatly improve the

sustainability of the PGG fishery (Kindsvater, Reynolds, Sadovy de

Mitcheson, & Mangel, 2017), it should be made clear that size limits

were only recommended, but not implemented in Belize for the

Atlantic goliath grouper (Graham, pers. comm. 2017). The Colombian

government declared in 2017 special management areas (Distritos

de Manejo Integrado) in two significant mangrove zones of the

Colombian Pacific (Cabo Manglares Bajo Mira y Frontera and El

Encanto de los Manglares del Bajo Baudó). This brings the opportunity

to give protection to PGG individuals prior to maturity in their nursery

habitats. The challenge facing these special management areas is to

actually achieve their conservation and sustainability goals, and not

just remain as parks on paper (see Rife, Erisman, Sanchez, & Aburto‐

Oropeza, 2013). It is equally important to give protection to spawning

aggregation sites, which need to be identified, as they are the sites

where spear fisheries are increasingly likely to operate and extract

large PGG. An additional management measure would be to impose

maximum and minimum size limits so that the fishery only affects a

small range of ages (Barnett et al., 2017). Finally, research addressing

poorly known aspects of the ecology and biology of PGG should

accompany the continuing conservation and management efforts. Of

special relevance are the identification of migration routes of juvenile

and adult PGG, and a stock assessment, with reliable growth rate,

abundance, and life‐history parameters for this species.

ACKNOWLEDGEMENTS

This project was funded by the Conservation Leadership Programme

(CLP), Rufford Foundation, and WWF Colombia. The fishing

communities at Jurubirá, El Valle, Bahía Solano, Arusí, and Bahía

Málaga were fundamental to the completion of this study. F. Pretel

and C. Pretel from Buenaventura fish market were crucial to obtaining

information about landings. C. Pretel and R. Fajardo kindly provided

some of the pictures shown in Figure 1. G.C.‐G. is sponsored by the

Alexander von Humboldt Foundation. Comments from two anony-

mous reviewers and the journal's chief editor are greatly appreciated.

ORCID

Gustavo A. Castellanos‐Galindo http://orcid.org/0000-0002-7849-

5205

REFERENCES

Aburto‐Oropeza, O., Erisman, B., Valdez‐Ornelas, V., & Danemann, G.(2008). Commercially important serranid fishes from the Gulf ofCalifornia: Ecology, fisheries, and conservation. Ciencia y Conservación,2008(1), 1–44.

Aguilar‐Perera, A., González‐Salas, C., Tuz‐Sulub, A., & Villegas‐Hernández,H. (2009). Fishery of the Goliath grouper, Epinephelus itajara (Teleostei:Epinephelidae) based on local ecological knowledge and fishery recordsin Yucatan, Mexico. Revista de Biología Tropical, 57(3), 557–566.

Baos, R., Castellanos‐Galindo, G. A., Chong‐Montenegro, C., Tompkins, P.,& Zapata, L. A. (2016). Length–weight relationship of the Pacific goliathgrouper, Epinephelus quinquefasciatus (Bocourt, 1868). Journal of AppliedIchthyology, 32(4), 727–728.

Barnett, L. A. K., Branch, T. A., Ranasinghe, R. A., & Essington, T. E. (2017).Old‐Growth Fishes Become Scarce under Fishing. Current Biology,27(18), 2843–2848.

Beaudreau, A. H., & Levin, P. S. (2014). Advancing the use of local ecologicalknowledge for assessing data‐poor species in coastal ecosystems.Ecological Applications, 24(2), 244–256.

Bullock, L. H., Murphy, M. D., Godcharles, M. F., & Mitchell, M. E. (1992).Age, growth, and reproduction of jewfish Epinephelus itajara in theeastern Gulf of Mexico. Fishery Bulletin, 90(2), 243–249.

Castellanos‐Galindo, G. A., Cantera, J., Saint‐Paul, U., & Ferrol‐Schulte, D.(2015). Threats to mangrove social‐ecological systems in the most lux-uriant coastal forests of the Neotropics. Biodiversity and Conservation,24(3), 701–704.

Castellanos‐Galindo, G. A., Baos, R., & Zapata, L. A. (2017). Epinephelusquinquefasciatus. In L. V. Chasqui, F. A. Polanco, P. A. Acero, P. A.Mejía‐Falla, A. Navia, L. A. Zapata, & J. P. Caldas (Eds.), Libro rojo depeces marinos de Colombia (pp. 432–436). Santa Marta, Colombia:Instituto de Investigaciones Marinas y Costeras INVEMAR, Ministeriode Ambiente y Desarrollo Sostenible.

Correa, I., & Morton, R. (2010). Pacific coast of Colombia. In E. C. F. Bird(Ed.), Encyclopedia of the world's coastal landforms (pp. 193–197).Dordrecht, the Netherlands: Springer.

Craig, M. T., Graham, R. T., Torres, R. A., Hyde, J. R., Freitas, M. O., Ferreira,B. P., … Robertson, D. R. (2009). How many species of Goliath Grouperare there? Cryptic genetic divergence in a threatened marine speciesand the resurrection of a geopolitical species. Endangered SpeciesResearch, 7(3), 167–174.

Craig, M. T., Sadovy de Mitcheson, Y. J., & Heemstra, P. C. (2011). Groupersof the World: A Field and Market Guide. Grahamstown, South Africa:NISC (Pty) Ltd.

Erisman, B. (2011). Epinephelus quinquefasciatus. In IUCN Red List ofThreatened Species v2011.2. Available at http://www.iucnredlist.org.Accessed on 29 May 2017.

Frias‐Torres, S. (2006). Habitat use of juvenile goliath grouper Epinephelusitajara in the Florida Keys, USA. Endangered Species Research, 2, 1–6.

Gaspari, L., Bryceson, I., & Kulindwa, K. (2015). Complementarity of fishers’traditional ecological knowledge and conventional science:

Page 10: Using landing statistics and fishers traditional ......data exist to complete any assessments for 30% of the species, and these are listed as Data Deficient (Sadovy de Mitcheson et

10 CASTELLANOS‐GALINDO ET AL.

Contributions to the management of groupers (Epinephelinae)fisheries around Mafia Island, Tanzania. Ocean & Coastal Management,114, 88–101.

Gerhardinger, L. C., Marenzi, R. C., Bertoncini, A. A., Medeiros, R. P., &Hostim‐Silva, M. (2006). Local Ecological Knowledge on the GoliathGrouper Epinephelus itajara (Teleostei: Serranidae) in Sourthern Brazil.Neotropical Ichthyology, 4(4), 441–450.

Giglio, V. J., Bertoncini, Á. A., Ferreira, B. P., Hostim‐Silva, M., & Freitas, M.O. (2014). Landings of goliath grouper, Epinephelus itajara, in Brazil:despite prohibited over ten years, fishing continues. Natureza &Conservação, 12(2), 118–123.

Glynn, P. W., & Ault, J. S. (2000). A biogeographic analysis and review of thefar eastern Pacific coral reef region. Coral Reefs, 19(1), 1–23.

Gómez, A. E., & Zapata, L. A. (1999). Generalidades sobre la pesquería ybiología de las chernas y meros (Pisces: Serranidae) en el Pacíficocolombiano. Boletín Científico INPA, 6(1), 227–246.

Graham, R. T., Rhodes, K. L., & Castellanos, D. (2009). Characterization ofthe Goliath Grouper Epinephelus itajara fishery of southern Belize forconservation planning. Endangered Species Research, 7, 195–204.

Heemstra, P. C., & Randall, J. E. (1993). Groupers of the World (Vol. 16).Rome, Italy: FAO Species Catalog.

Heyman, W. D., & Graham, R. T. (2000a). The Voice of the Fishermen ofSouthern Belize. Punta Gorda, Belize: Toledo Institute for Developmentand Environment (TIDE) & Trinational Alliance for the Gulf of Honduras(TRIGOH).

Heyman, W. D., & Graham, R. T. (2000b). La Voz de los Pescadores de laCosta Atlántica de Honduras. Tela, Honduras: Prolansate.

Heyman, W. D., & Graham, R. T. (2000c). La Voz de los Pescadores de laCosta Atlántica de Guatemala. Ciudad de Guatemala, Guatemala:FUNDAECO.

Hind, E. J. (2015). A review of the past, the present, and the future offishers’ knowledge research: A challenge to established fisheriesscience. ICES Journal of Marine Sciences, 72(2), 341–358.

Hixon, M. A., & Carr, M. H. (1997). Synergistic predation, density depen-dence, and population regulation in marine fish. Science, 277(5328),946–949.

Hixon, M. A., Johnson, D. W., & Sogard, S. M. (2014). BOFFFFs: On theimportance of conserving old‐growth age structure in fishery popula-tions. ICES Journal of Marine Science, 71(8), 2171–2185.

Johannes, R. E. (1998). The case of data‐less marine resource management:examples from tropical nearshore fin fisheries. Trends in Ecology andEvolution, 13(6), 243–246.

Kindsvater, H. K., Reynolds, J. D., Sadovy de Mitcheson, Y., & Mangel, M.(2017). Selectivity matters: Rules of thumb for management of plate‐sized, sex‐changing fish in the live reef food fish trade. Fish andFisheries, 18(5), 821–836.

Koenig, C. C., Coleman, F. C., Eklund, A. M., Schull, J., & Ueland, J. (2007).Mangroves as essential nursery habitat for goliath grouper (Epinephelusitajara). Bulletin of Marine Science, 80(3), 567–586.

MADR (Ministerio de Agricultura y Desarrollo Rural) & CCI (CorporaciónColombia Internacional). (2011). Pesca y Acuicultura Colombia 2010.Bogotá, Columbia: Corporación Colombia Internacional.

Meisel Roca, A., & Pérez V, G. J. (2006). Geografía física y poblamiento en lacosta Caribe Colombiana. Documentos de trabajo sobre economíaregional, 73, 1–79.

Mejía, L., & Acero, A. (2002). Libro rojo de peces marinos de Colombia. La serieLibros Rojos de Especies Amenazadas de Colombia. Bogotá, Colombia:INVEMAR, Instituto de Ciencias Naturales – Universidad Nacional deColombia, and Ministerio del Medio Ambiente.

Pereira‐Velásquez, F. (1993). La pesca en el Pacífico. In P. Leyva (Ed.),Colombia, Pacífico, Tomo II. Proyecto Biopacífico. Santa Fe de Bogotá,Colombia: Fondo para la Protección del Medio Ambiente, FEN.

Polidoro, B. A., Brooks, T., Carpenter, K. E., Edgar, G. J., Henderson, S.,Sanciangco, J., & Robertson, D. R. (2012). Patterns of extinction riskand threat for marine vertebrates and habitat‐forming species in theTropical Eastern Pacific. Marine Ecology Progress Series, 448, 93–104.

Poveda, G., & Mesa, O. J. (2000). On the existence of Lloró (the rainiestlocality on Earth): Enhanced ocean‐land‐atmosphere interaction by alow‐level jet. Geophysical Research Letters, 27(11), 1675–1678.

Ramírez, J. J. C., & de Aguas, P.,. J. M. (2015). Escalafón de la competitividadde los departamentos de Colombia 2015. Santiago de Chile, Chile: CEPALNaciones Unidas.

Rife, A. N., Erisman, B., Sanchez, A., & Aburto‐Oropeza, O. (2013). Whengood intentions are not enough… Insights on networks of “paper park”marine protected areas. Conservation Letters, 6(3), 200–212.

Sadovy, Y., & Eklund, A. (1999). Synopsis of Biological Data on the NassauGrouper, Ephinephelus striatus, and the Jewfish, E. itajara. NOAATechnical Report. Seattle, Washington, USA: University of CaliforniaLibraries.

Sadovy de Mitcheson, I., Craig, M. T., Bertoncini, A. A., Carpenter, K. E.,Cheung, W. W. L., Choat, J. H., … Sanciangco, J. (2013). Fishinggroupers towards extinction: A global assessment on threats andextinction risks in a billion dollar fishery. Fish and Fisheries, 14(2),119–133.

Sáenz‐Arroyo, A., Roberts, C. M., Torre, J., Cariño‐Olvera, M., & Enriquez‐Andrade, R. R. (2005). Rapidly shifting environmental baselines amongfishers of the Gulf of California. Proceedings of the Royal Society ofLondon B, 272(1575), 1957–1962.

Stewart, B. D., & Jones, G. P. (2001). Associations between the abundanceof piscivorous fishes and their prey on coral reefs: Implications forprey‐fish mortality. Marine Biology, 138(2), 383–397.

Wielgus, J., Zeller, D., Caicedo‐Herrera, D., & Sumaila, R. (2010). Estimationof fisheries removals and primary economic impact of the small‐scaleand industrial marine fisheries in Colombia. Marine Policy, 34(3),506–513.

How to cite this article: Castellanos‐Galindo GA, Chong‐

Montenegro C, Baos E RA, et al. Using landing statistics and

fishers’ traditional ecological knowledge to assess conservation

threats to Pacific goliath grouper in Colombia. Aquatic Conserv:

Mar Freshw Ecosyst. 2018;1–10. https://doi.org/10.1002/

aqc.2871